Klebsiella michiganensis transmission enhances resistance to Enterobacteriaceae gut invasion by nutrition competition

Nat Microbiol. 2020 Apr;5(4):630-641. doi: 10.1038/s41564-019-0658-4. Epub 2020 Jan 20.

Abstract

Intestinal microbiotas contain beneficial microorganisms that protect against pathogen colonization; treatment with antibiotics disrupts the microbiota and compromises colonization resistance. Here, we determine the impact of exchanging microorganisms between hosts on resilience to the colonization of invaders after antibiotic-induced dysbiosis. We assess the functional consequences of dysbiosis using a mouse model of colonization resistance against Escherichia coli. Antibiotics caused stochastic loss of members of the microbiota, but the microbiotas of co-housed mice remained more similar to each other compared with the microbiotas among singly housed animals. Strikingly, co-housed mice maintained colonization resistance after treatment with antibiotics, whereas most singly housed mice were susceptible to E. coli. The ability to retain or share the commensal Klebsiella michiganensis, a member of the Enterobacteriaceae family, was sufficient for colonization resistance after treatment with antibiotics. K. michiganensis generally outcompeted E. coli in vitro, but in vivo administration of galactitol-a nutrient that supports the growth of only E. coli-to bi-colonized gnotobiotic mice abolished the colonization-resistance capacity of K. michiganensis against E. coli, supporting the idea that nutrient competition is the primary interaction mechanism. K. michiganensis also hampered colonization of the pathogen Salmonella, prolonging host survival. Our results address functional consequences of the stochastic effects of microbiota perturbations, whereby microbial transmission through host interactions can facilitate reacquisition of beneficial commensals, minimizing the negative impact of antibiotics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Bacteroidetes / classification
  • Bacteroidetes / isolation & purification
  • Ciprofloxacin / pharmacology
  • Colony Count, Microbial
  • Dysbiosis / chemically induced
  • Dysbiosis / microbiology*
  • Escherichia coli / drug effects
  • Escherichia coli / growth & development
  • Escherichia coli / pathogenicity
  • Firmicutes / classification
  • Firmicutes / isolation & purification
  • Gastrointestinal Microbiome / physiology*
  • Germ-Free Life
  • Klebsiella / drug effects
  • Klebsiella / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microbial Interactions*
  • Salmonella typhimurium / drug effects
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / pathogenicity
  • Streptomycin / pharmacology
  • Symbiosis / physiology*
  • Verrucomicrobia / classification
  • Verrucomicrobia / isolation & purification

Substances

  • Anti-Bacterial Agents
  • Ciprofloxacin
  • Streptomycin

Supplementary concepts

  • Klebsiella michiganensis